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Facets and mechanisms of adaptive pain behavior: predictive regulation and action.

Morrison I, Perini I, Dunham J - Front Hum Neurosci (2013)

Bottom Line: Regulatory processes occur on many levels, and can be dynamically influenced by local interactions or by modulation from other brain areas in the network.The PRA model centers on neural substrates supporting the predictive nature of pain processing, as well as on finely-calibrated yet versatile regulatory processes that ultimately affect behavior.We outline several operational categories of pain behavior, from spinally-mediated reflexes to adaptive voluntary action, situated at various neural levels.

View Article: PubMed Central - PubMed

Affiliation: 1Department of Clinical Neurophysiology, Sahlgrenska University Hospital Gothenburg, Sweden ; 2Institute of Neuroscience and Physiology, University of Gothenburg Gothenburg, Sweden ; 3Department of Cognitive Neuroscience and Philosophy, University of Skövde Skövde, Sweden.

ABSTRACT
Neural mechanisms underlying nociception and pain perception are considered to serve the ultimate goal of limiting tissue damage. However, since pain usually occurs in complex environments and situations that call for elaborate control over behavior, simple avoidance is insufficient to explain a range of mammalian pain responses, especially in the presence of competing goals. In this integrative review we propose a Predictive Regulation and Action (PRA) model of acute pain processing. It emphasizes evidence that the nervous system is organized to anticipate potential pain and to adjust behavior before the risk of tissue damage becomes critical. Regulatory processes occur on many levels, and can be dynamically influenced by local interactions or by modulation from other brain areas in the network. The PRA model centers on neural substrates supporting the predictive nature of pain processing, as well as on finely-calibrated yet versatile regulatory processes that ultimately affect behavior. We outline several operational categories of pain behavior, from spinally-mediated reflexes to adaptive voluntary action, situated at various neural levels. An implication is that neural processes that track potential tissue damage in terms of behavioral consequences are an integral part of pain perception.

No MeSH data available.


Related in: MedlinePlus

(A) Analysis of fMRI data comparing blood-oxygen-level-dependent (BOLD) responses to stimulation across sensory domains (vision, audition, somatosensation, and pain), indicating that multimodal activity accounts for most of the cortical network activation during pain (Wiech et al., 2010). (B) EEG results demonstrating that cortical responses to Aδ and C nociceptor activation by laser-evoked potential (LEP) stimulation reflects predominantly multimodal and to some extent somatosensory–specific activity, but limited nociceptive-specific activity (Fuster, 1991). (C) fMRI evidence demonstrating correlations in regions of midcingulate cortex (MCC) with individual motor reactivity in the spinal RIII reflex (top) and variance in autonomic arousal (bottom) during electrical pain stimulation (Bancaud et al., 1976). (D) fMRI evidence demonstrates that midcingulate but not anterior insula activations during pain are contingent on motor processing (Duerden and Albanese, 2013). Figures reproduced with permission.
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Figure 3: (A) Analysis of fMRI data comparing blood-oxygen-level-dependent (BOLD) responses to stimulation across sensory domains (vision, audition, somatosensation, and pain), indicating that multimodal activity accounts for most of the cortical network activation during pain (Wiech et al., 2010). (B) EEG results demonstrating that cortical responses to Aδ and C nociceptor activation by laser-evoked potential (LEP) stimulation reflects predominantly multimodal and to some extent somatosensory–specific activity, but limited nociceptive-specific activity (Fuster, 1991). (C) fMRI evidence demonstrating correlations in regions of midcingulate cortex (MCC) with individual motor reactivity in the spinal RIII reflex (top) and variance in autonomic arousal (bottom) during electrical pain stimulation (Bancaud et al., 1976). (D) fMRI evidence demonstrates that midcingulate but not anterior insula activations during pain are contingent on motor processing (Duerden and Albanese, 2013). Figures reproduced with permission.

Mentions: A recent activation-likelihood-estimate (ALE) meta-analysis of fMRI studies showed that the anterior cingulate cortex (ACC) is the region most likely to be activated by acute pain (Duerden and Albanese, 2013). Although the cingulate cortex is often regarded as a key area in a “pain neuromatrix”, a specific role in pain is unlikely, since it is also implicated in a range of non-pain-related functions (Mouraux and Iannetti, 2009). At the cortical level, even somatosensory contribution to pain processing may be small, and nociceptive-specific contribution even smaller, compared to multimodal processing in networks throughout the brain (Mouraux and Iannetti, 2009; Mouraux et al., 2011; Figure 3).


Facets and mechanisms of adaptive pain behavior: predictive regulation and action.

Morrison I, Perini I, Dunham J - Front Hum Neurosci (2013)

(A) Analysis of fMRI data comparing blood-oxygen-level-dependent (BOLD) responses to stimulation across sensory domains (vision, audition, somatosensation, and pain), indicating that multimodal activity accounts for most of the cortical network activation during pain (Wiech et al., 2010). (B) EEG results demonstrating that cortical responses to Aδ and C nociceptor activation by laser-evoked potential (LEP) stimulation reflects predominantly multimodal and to some extent somatosensory–specific activity, but limited nociceptive-specific activity (Fuster, 1991). (C) fMRI evidence demonstrating correlations in regions of midcingulate cortex (MCC) with individual motor reactivity in the spinal RIII reflex (top) and variance in autonomic arousal (bottom) during electrical pain stimulation (Bancaud et al., 1976). (D) fMRI evidence demonstrates that midcingulate but not anterior insula activations during pain are contingent on motor processing (Duerden and Albanese, 2013). Figures reproduced with permission.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3842910&req=5

Figure 3: (A) Analysis of fMRI data comparing blood-oxygen-level-dependent (BOLD) responses to stimulation across sensory domains (vision, audition, somatosensation, and pain), indicating that multimodal activity accounts for most of the cortical network activation during pain (Wiech et al., 2010). (B) EEG results demonstrating that cortical responses to Aδ and C nociceptor activation by laser-evoked potential (LEP) stimulation reflects predominantly multimodal and to some extent somatosensory–specific activity, but limited nociceptive-specific activity (Fuster, 1991). (C) fMRI evidence demonstrating correlations in regions of midcingulate cortex (MCC) with individual motor reactivity in the spinal RIII reflex (top) and variance in autonomic arousal (bottom) during electrical pain stimulation (Bancaud et al., 1976). (D) fMRI evidence demonstrates that midcingulate but not anterior insula activations during pain are contingent on motor processing (Duerden and Albanese, 2013). Figures reproduced with permission.
Mentions: A recent activation-likelihood-estimate (ALE) meta-analysis of fMRI studies showed that the anterior cingulate cortex (ACC) is the region most likely to be activated by acute pain (Duerden and Albanese, 2013). Although the cingulate cortex is often regarded as a key area in a “pain neuromatrix”, a specific role in pain is unlikely, since it is also implicated in a range of non-pain-related functions (Mouraux and Iannetti, 2009). At the cortical level, even somatosensory contribution to pain processing may be small, and nociceptive-specific contribution even smaller, compared to multimodal processing in networks throughout the brain (Mouraux and Iannetti, 2009; Mouraux et al., 2011; Figure 3).

Bottom Line: Regulatory processes occur on many levels, and can be dynamically influenced by local interactions or by modulation from other brain areas in the network.The PRA model centers on neural substrates supporting the predictive nature of pain processing, as well as on finely-calibrated yet versatile regulatory processes that ultimately affect behavior.We outline several operational categories of pain behavior, from spinally-mediated reflexes to adaptive voluntary action, situated at various neural levels.

View Article: PubMed Central - PubMed

Affiliation: 1Department of Clinical Neurophysiology, Sahlgrenska University Hospital Gothenburg, Sweden ; 2Institute of Neuroscience and Physiology, University of Gothenburg Gothenburg, Sweden ; 3Department of Cognitive Neuroscience and Philosophy, University of Skövde Skövde, Sweden.

ABSTRACT
Neural mechanisms underlying nociception and pain perception are considered to serve the ultimate goal of limiting tissue damage. However, since pain usually occurs in complex environments and situations that call for elaborate control over behavior, simple avoidance is insufficient to explain a range of mammalian pain responses, especially in the presence of competing goals. In this integrative review we propose a Predictive Regulation and Action (PRA) model of acute pain processing. It emphasizes evidence that the nervous system is organized to anticipate potential pain and to adjust behavior before the risk of tissue damage becomes critical. Regulatory processes occur on many levels, and can be dynamically influenced by local interactions or by modulation from other brain areas in the network. The PRA model centers on neural substrates supporting the predictive nature of pain processing, as well as on finely-calibrated yet versatile regulatory processes that ultimately affect behavior. We outline several operational categories of pain behavior, from spinally-mediated reflexes to adaptive voluntary action, situated at various neural levels. An implication is that neural processes that track potential tissue damage in terms of behavioral consequences are an integral part of pain perception.

No MeSH data available.


Related in: MedlinePlus